A Tale of Two Flagella

They are the best of beings; they are the worst of beings. They are animals; they are plants. They are saviors; they are killers. They are predators; they are parasites. They are, in short, dinoflagellates — a large, diverse and eccentric group of (usually) single-celled organisms that are as celebrated as they are feared. And I hereby nominate them for Life-form of the Month: January.

If you were to look at a dinoflagellate through a microscope, you might see anything from a small brown ball to an elaborate structure with whorls and spines — that depends on the species. All dinoflagellates live in water, most famously the ocean (though some live in freshwater), and many of them can swim: protruding from their outsides they have two whip-like structures known as flagella, one for moving and one for steering. (Flagella is plural: if they had only one, they’d have a flagellum.)

Some dinoflagellates have eyes. Others give off light. Some, like plants, make energy from the sun; others, like animals, capture and eat their prey. Some do both. Funky.

But even if you’ve never seen a dinoflagellate and wouldn’t recognize one if it waved its flagella at you, you’ve probably come across them, for they impinge on our lives in two important ways, one good, one bad.
Good: they make coral reefs possible. Most reef corals are associations between an animal (which makes the stony structures we think of as reef) and dinoflagellates from a lineage known as Symbiodinium. These are in the “plant” camp; they make energy from the sun. In return for shelter and some minerals, they provide their host with food: in some cases, dinoflagellates provide as much as 90 percent of the coral’s nutrition.

Dinoflagellates are not passed from parent to child like family diamonds; instead, baby corals get them from the water. Which coral gets what can be a flexible affair, with corals of the same species sometimes housing different dinoflagellates, and dinoflagellates of a given species being able to shack up with different corals.

How corals and dinoflagellates “choose” each other is unclear, but the details of the association do matter: different dinoflagellates cause corals to grow at different speeds, and allow them to grow in water of different temperatures. In one experiment, for example, juvenile corals of the species Acropora tenuis grew twice as fast when they had dinoflagellates from a group known as Symbiodinium C1 than when they were lumbered with those from Symbiodinium D. However, corals that contain Symbiodinium D dinoflagellates are better able to cope with warmer waters.

Which has important implications. Corals are sensitive to temperature: an increase of a few degrees above the usual summer temperatures can kill them. As the water warms, the relationship between the animal and the dinoflagellate often breaks down, and the corals turn white, a phenomenon known as coral bleaching. When this happens — and it’s been happening a lot recently — the corals may die. Yet on any given bleached reef, some corals make it through; the difference comes down to their dinoflagellates. Whether it’s possible to help corals survive bleaching by manipulating their dinoflagellates isn’t known. But, as sea temperatures rise around the world, it’s tempting to hope that heat-tolerant dinoflagellates will be the saviors of coral reefs.

Not all dinoflagellates are so helpful, however. Pick up a copy of the journal Harmful Algae, and you’ll find plenty of articles about how dangerous some dinoflagellates can be. Many species make powerful nerve poisons; these can become concentrated in the flesh of fish and shellfish, and harm anyone who happens to eat the contaminated animals. Two of the most notorious syndromes caused by dinoflagellates are ciguatera fish poisoning and paralytic shellfish poisoning; both can make you very ill, and may even kill you.

Further denting their reputation, some dinoflagellates are responsible for “red tides,” or “harmful algal blooms.” During a harmful bloom, toxic dinoflagellates accumulate in huge numbers, with devastating consequences on other beings. For example, in the Gulf of Mexico, blooms of the dinoflagellate Karenia brevis regularly kill dolphins, turtles, manatees, some seabirds and massive numbers of fish; they also send humans to the hospital for breathing problems and stomach upsets.

Nasty stuff. But put aside the harmful and helpful aspects of dinoflagellates and, for a moment, consider just how plain weird these organisms are. Especially since they are not some relict life form, but highly evolved beings whose closest cousins are the apicomplexans — a group that includes the bugs that cause malaria.

Most dinoflagellates are small — you need a microscope to see them — and even the biggest ones are no bigger than a piece of caviar. But they have gigantic genomes. Some dinoflagellates have genomes containing around 67 times more DNA than the human genome, and 10 times more than the most extravagantly endowed plants. That’s colossal. (Note that lots of DNA doesn’t necessarily mean lots of genes; in terms of gene numbers, it remains to be seen if dinoflagellates are exceptional.)

Even more peculiar is the way they store their DNA. The usual way is to wrap it around molecular spools known as histones. Dinoflagellates don’t have histones. Instead, their genome appears to exist as a liquid crystal matrix. Wackier still: dinoflagellates have unconventional DNA. In most organisms, DNA is composed of the molecules adenine, guanine, cytosine and thymine. Dinoflagellates often replace thymine with something called hydroxymethyluracil. It’s all most bizarre.

Then there’s this business of photosynthesis — making energy from the sun. Different lineages of dinoflagellates appear to have acquired this ability several times independently. But it isn’t because they’ve evolved photosynthesis over and over again. Instead, they have a strange knack for engulfing other photosynthetic organisms and taking over their chloroplasts — the entities that actually do the work of transforming sunbeams into energy. To put it in context, in all of the rest of the tree of life, such engulfments are thought to have happened between three and six times. In dinoflagellates, it’s happened five times at least. Why are they so good at it? No one knows.

In short: dinoflagellates may be small, but they are among the most versatile and peculiar organisms on the planet. Here’s to a further unraveling of their mysteries!

Notes:

For an excellent overview of the weirdness of dinoflagellates, see Hackett, J. D. et al. 2004. “Dinoflagellates: a remarkable evolutionary experiment.” American Journal of Botany 91: 1523-1534.

For the experiment showing coral growth depends on its dinoflagellates, see Little, A. F., van Oppen, M. J. H. and Willis, B. L. 2004. “Flexibility in algal endosymbioses shapes growth in reef corals.” Science 304: 1492-1494. For the an overview of rising water temperature and the problem of coral bleaching, see Hughes, T. P. et al. 2003. “Climate change, human impacts, and the resilience of coral reefs.” Science 301: 929-933. Several papers have shown that particular strains of dinoflagellates help corals to weather bleaching events. See, for example, Baker, A. C. et al. 2004. “Corals’ adaptive response to climate change.” Nature 430: 741; Berkelmans, R. and van Oppen, M. J. H. 2006. “The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change.” Proceedings of the Royal Society of London B 273: 2305-2312 (this paper also provides information and references on the proportion of nutrients that the dinoflagellates provide their hosts); and LaJeunesse, T. C. et al. 2009. “Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Carribean mass coral ‘bleaching’ event.” Proceedings of the Royal Society of London B 276: 4139-4148.

For a fascinating account of dinoflagellate genome organization, including genome size, the lack of histones and the presence of the liquid crystal matrix, see Moreno Díaz de la Espina, S. et al. 2005. “Organization of the genome and gene expression in a nuclear environment lacking histones and nucleosomes: the amazing dinoflagellates.” European Journal of Cell Biology 84: 137-149. For the replacement of thymine with hydroxymethyluracil, see Rae, P. M. M. 1976. “Hydroxymethyluracil in eukaryote DNA: a natural feature of the Pyrrophyta (Dinoflagellates).” Science 194: 1062-1064.

Counting how often chloroplasts have been captured is a tricky affair; one set of estimates is given by the Hackett et al. 2004 paper listed above; see also Shalchian-Tabrizi, K. et al. 2006. “Heterotachy processes in rhodophyte-derived secondhand plastid genes: implications for addressing the origin and evolution of dinoflagellate plastids.” Molecular Biology and Evolution 23: 1504-1515; and Schnepf, E. and Elbrächter, M. 1999. “Dinophyte chloroplasts and phylogeny — a review.” Grana 38: 81-97.

Many thanks to Tsvetan Bachvaroff for discussing dinoflagellates and answering a slew of questions, and to Jonathan Swire for comments and suggestions.

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Olivia Judson, an evolutionary biologist, writes every Wednesday about the influence of science and biology on modern life. She is the author of “Dr. Tatiana’s Sex Advice to All Creation: The Definitive Guide to the Evolutionary Biology of Sex.” Ms. Judson has been a reporter for The Economist and has written for a number of other publications, including Nature, The Financial Times, The Atlantic and Natural History. She is a research fellow in biology at Imperial College London.